Chin J Plant Ecol ›› 2019, Vol. 43 ›› Issue (3): 217-226.doi: 10.17521/cjpe.2019.0003

• Research Articles • Previous Articles     Next Articles

Effects of functional diversity and phylogenetic diversity on the tropical cloud forest community assembly

CHENG Yi-Kang1,ZHANG Hui1,WANG Xu1,LONG Wen-Xing1,2,*(),LI Chao1,FANG Yan-Shan3,FU Ming-Qi3,ZHU Kong-Xin4   

  1. 1 Institute of Tropical Agriculture and Forestry, Hainan University, Haikou 570228, China
    2 National Positioning Observation and Research Station of Forest Ecosystem, Wuzhishan, Hainan 572200, China
    3 Administration of Limushan Provincial Natural Reserve, Qiongzhong, Hainan 572900, China
    4 Forestry Bureau of Bawangling, Changjiang, Hainan 572700, China
  • Received:2019-01-04 Revised:2019-02-27 Online:2019-05-30 Published:2019-03-20
  • Contact: LONG Wen-Xing ORCID:0000-0002-9195-5878 E-mail:oklong@hainanu.edu.cn
  • Supported by:
    Supported by the National Natural Science Foundation of China(31660163);Supported by the National Natural Science Foundation of China(31870508);The Natural Science Foundation of Hainan Province, China(312064);The Natural Science Foundation of Hainan Province, China(2016CXTD003D)

Abstract:

Aims Phylogenetic and functional diversity are important components of species biodiversity, and are thought to play key roles in the mechanisms of community assembly. In this study, we explore the mechanisms of community assembly in tropical cloud forest plant community in Hainan Island, in southern China, using phylogenetic and functional diversity based methods.


Methods We constructed a species pool of 186 woody plant species from three tropical cloud forest sites in Hainan Island. For these species, we measured 13 functional traits and assessed their phylogenetic signals. In addition, we measured seven environmental factors and assessed their relationships using Principal component analysis (PCA). Then we chose Rao’s quadratic entropy (RaoQ) and mean pairwise distance (MPD) indices to examine the effects of functional diversity and phylogenetic diversity on tropical cloud forest community assembly. To do this we compared these indices to expectations under null models that assume neutral community assembly. We used standard effect sizes to evaluate the influence of environmental factors on community assembly.


Important findings Canopy openness, soil total phosphorus content and slope were significant environmental predictors in tropical cloud forest. The phylogenetic signals of most functional traits were very low and not significant, indicating that the phylogenetic relationship and functional traits were not consistent with the change of historical process. The observed values of RaoQ and MPD were significantly lower than expected, and their standard effect sizes were significantly correlated with soil phosphorus content, which suggested that habitat filtering driven by soil phosphorus was the key factor driving the community assembly in tropical cloud forest.

Key words: community assembly, functional diversity, phylogenetic diversity, environment factor, tropical cloud forest

Fig. 1

Distribution of the tropical cloud forest study sites in Hainan Island."

Table 1

Information on the study sites in the tropical cloud forest in Hainan Island"

研究样地
Study site
海拔
Elevation (m)
经度
Longitude (E)
纬度
Latitude (N)
坡度
Slope (°)
样方数
No. of plots
样地面积
Plot area (m2)
优势种
Dominant species
尖峰岭
Jianfeng Mt.
1 187.17-
1 397.19
108.87° 18.72° 10-65 12 4 800 罗浮锥、丛花厚壳桂、美丽新木姜子、黄叶树 Castanopsis faberi, Cryptocarya densiflora, Neolitsea pulchella, Xanthophyllum hainanense
霸王岭
Bawang Mt.
1 313.24-
1 385.24
109.21° 19.08° 2-45 21 8 400 蚊母树、赤楠、九节、黄杞
Distylium racemosum, Syzygium buxifolium,
Psychotria rubra, Engelhardtia roxburghiana
黎母山
Limu Mt.
1 363.73-
1 403.32
109.76° 19.18° 3-42 15 6 000 普洱茶、岭南青冈、罗浮锥、细枝柃
Camellia sinensis var. assamica, Cyclobalanopsis championii, Castanopsis faberi, Eurya loquaiana

Table 2

Principle component analysis (PCA) among environment factors in tropical cloud forest"

环境变量 Environmental variable PCA1 PCA2 PCA3 PCA4
林冠开阔度 CO (%) -0.33 - 0.89 -0.24
土壤有机质含量 SOM (g·kg-1) -0.35 0.47 -0.23 -0.34
全磷含量 TP (g·kg-1) -0.50 - - 0.31
全氮含量 TN (g·kg-1) -0.47 -0.11 -0.32 -0.15
有效氮含量 AN (mg·kg-1) -0.47 -0.19 -0.19 -0.19
有效磷含量 AP (mg·kg-1) 0.24 0.59 - -0.48
坡度 SP (o) 0.13 -0.61 - -0.66
特征值 Characteristic value 3.32 1.87 0.48 0.17
解释方差比例 Explained variance proportion 0.52 0.27 0.10 0.07
累积解释方差比例 Cumulative explained variance proportion 0.52 0.79 0.89 0.96

Fig. 2

Correlation analysis among environmental factors of Hainan tropical cloud forests. CO, canopy openness; SOM, soil organic matter content; TP, total phosphorus content; TN, total nitrogen content; AN, available nitrogen content; AP, available phosphorus content; SP, slope. *, p < 0.05; **, p < 0.01; ***, p < 0.001."

Table 3

Phylogenetic signal of plants functional traits in tropical cloud forest"

功能性状 Functional trait K p
根部氮含量 Root nitrogen content (RN) 0.258 0.639
根部磷含量 Root phosphorus content (RP) 0.405 0.193
根部可溶性糖含量 Root soluble sugar content (RS) 0.210 0.820
叶片氮含量 Leaf nitrogen content (LN) 0.677 0.027
叶片磷含量 Leaf phosphorus content (LP) 0.579 0.055
叶片可溶性糖含量 Leaf soluble sugar content (LS) 0.190 0.857
茎干氮含量 Stem nitrogen content (SN) 0.448 0.195
茎干磷含量 Stem phosphorus content (SP) 4.258 0.005
茎干可溶性糖含量 Stem soluble sugar content (SS) 0.314 0.429
比叶面积 Specific leaf area (SLA) 0.373 0.413
叶绿素含量 Chlorophyll content (Chl) 0.459 0.062
叶片厚度 Leaf thickness (LTh) 0.282 0.589
木材密度 Wood density (WD) 0.294 0.527

Fig. 3

Comparison of functional diversity and phylogenetic diversity expectations with observed values in tropical cloud forest. The null distribution is the grey histogram and the observed values are the black vertical bars. MPD, mean pairwise distance; RaoQ, Rao’s quadratic entropy."

Fig. 4

Patterns of standard effect size of Rao’s quadratic entropy (SES.RaoQ) along environmental gradients in tropical cloud forest. CO, canopy openness; TP, total phosphorus content; SP, slope."

Fig. 5

Patterns of net relatedness index (NRI) along environmental gradients in tropical cloud forest. CO, canopy openness; TP, total phosphorus content; SP, slope."

[1] Agricultural Chemistry Committee of Soil Society of China ( 1983). Agricultural chemical Routine Analysis Method of Soil. Science Press, Beijing. 186-194.
[ 中国土壤学会农业化学专业委员会( 1983). 土壤农业化学常规分析方法. 科学出版社, 北京. 186-194.]
[2] Andersen KM, Endara MJ, Turner BL, Dalling JW ( 2012). Trait-based community assembly of understory palms along a soil nutrient gradient in a lower montane tropical forest. Oecologia, 168, 519-531.
[3] Blomberg SP, Garland T, Ives AR ( 2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717-745.
[4] Botta-Dukát Z, Czúcz B ( 2016). Testing the ability of functional diversity indices to detect trait convergence and divergence using individual-based simulation. Methods in Ecology and Evolution, 7, 114-126.
[5] Bu WS, Zang RG, Ding Y ( 2014). Field observed relationships between biodiversity and ecosystem functioning during secondary succession in a tropical lowland rainforest. Acta Oecologica, 55, 1-7.
[6] Cadotte MW, Cardinale BJ, Oakley TH ( 2008). Evolutionary history and the effect of biodiversity on plant productivity. Proceedings of the National Academy of Sciences of the United States of America, 105, 17012-17017.
[7] Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW ( 2009). The merging of community ecology and phylogenetic biology. Ecology Letters, 12, 693-715.
[8] CBOL Plant Wording Group ( 2009). A DNA barcode for land plants. Proceedings of the National Academy of Sciences of the United States of America, 106, 12794-12797.
[9] Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, Steege H, Morgan HD, Heijden A, Pausas JG, Poorter H ( 2003). A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany, 51, 335-380.
[10] Cornell HV ( 1985). Local and regional richness of cynipine gall wasps on California oaks. Ecology, 66, 1247-1260.
[11] Cornell HV, Harrison SP ( 2014). What are species pools and when are they important? Annual Review of Ecology, Evolution,and Systematics, 45, 45-67.
[12] de Bello F, Price JN, Münkemüller T, Liira J, Zobel M, Thuiller W, Gerhold P, Götzenberger L, Lavergne S, Lepš S, Zobel K, Pärtel M ( 2012). Functional species pool framework to test for biotic effects on community assembly. Ecology, 93, 2263-2273.
[13] Eller CB, Burgess SSO, Oliveira RS ( 2015). Environmental controls in the water use patterns of a tropical cloud forest tree species, Drimys brasiliensis (Winteraceae). Tree Physiology, 35, 387-399.
[14] Eriksson O ( 1993). The species-pool hypothesis and plant community diversity. Oikos, 68, 371-374.
[15] Goldsmith GR, Matzke NJ, Dawson TE ( 2013). The incidence and implications of clouds for cloud forest plant water relations. Ecology Letters, 16, 307-314.
[16] Gonzalez-Caro S, Umana MN, Alvarez E, Stevenson PR, Swenson NG ( 2014). Phylogenetic alpha and beta diversity in tropical tree assemblages along regional-scale environmental gradients in northwest South America. Journal of Plant Ecology, 7, 145-153.
[17] Hardy OJ ( 2008). Testing the spatial phylogenetic structure of local communities: Statistical performances of different null models and test statistics on a locally neutral community. Journal of Ecology, 96, 914-926.
[18] Harrison S, Cornell H ( 2008). Toward a better understanding of the regional causes of local community richness. Ecology Letters, 11, 969-979.
[19] He JS, Wang X, Flynn DFB, Wang L, Schmid B, Fang J ( 2009). Taxonomic, phylogenetic, and environmental trade-offs between leaf productivity and persistence. Ecology, 90, 2779-2791.
[20] Kang Y, Deng Z, Zang R, Long W ( 2017). DNA barcoding analysis and phylogenetic relationships of tree species in tropical cloud forests. Scientific Reports, 7, 12564. DOI: 10.1038/s41598-017-13057-0.
[21] Kraft NJB, Ackerly DD ( 2010). Functional trait and phylogenetic tests of community assembly across spatial scales in an Amazonian forest. Ecological Monographs, 80, 401-422.
[22] Kraft NJB, Valencia R, Ackerly DD ( 2008). Functional traits and niche-based tree community assembly in an Amazonia forest. Science, 322, 580-582.
[23] Long WX, Schamp BS, Zang RG, Ding Y, Huang YF, Xiang YZ ( 2015 a). Community assembly in a tropical cloud forest related to specific leaf area and maximum species height. Journal of Vegetation Science, 47, 416-423.
[24] Long WX, Xiong MH, Zang RG, Schamp BS, Yang XB, Ding Y, Huang YF, Xiang YZ ( 2015 b). Changes in patterns of species co-occurrence across two tropical cloud forests differing in soil nutrients and air temperature. Biotropica, 47, 416-423.
[25] Long WX, Zang RG, Ding Y ( 2011 a). Air temperature and soil phosphorus availability correlate with trait differences between two types of tropical cloud forests. Flora, 206, 896-903.
[26] Long WX, Zang RG, Schamp BS, Ding Y ( 2011 b). Within- and among-species variation in specific leaf area drive community assembly in a tropical cloud forest. Oecologia, 167, 1103-1113.
[27] Losos JB ( 2008). Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters, 11, 995-1007.
[28] Luna-Vega I, Magallón S ( 2010). Phylogenetic composition of angiosperm diversity in the cloud forests of Mexico. Biotropica, 42, 444-454.
[29] Mason NWH, Richardson SJ, Peltzer DA, Bello FD, Wardle DA, Allen RB ( 2012). Changes in coexistence mechanisms along a long-term soil chronosequence revealed by functional trait diversity. Journal of Ecology, 100, 678-689.
[30] McGill BJ, Enquist BJ, Weiher E, Westoby M ( 2006). Rebuilding community ecology from functional traits. Trends in Ecology & Evolution, 21, 178-185.
[31] McIntire EJB, Fajardo A ( 2014). Facilitation as a ubiquitous driver of biodiversity. New Phytologist, 201, 403-416.
[32] Mori AS, Shiono T, Koide D, Kitagawa R, Ota AT, Mizumachi E ( 2013). Community assembly processes shape an altitudinal gradient of forest biodiversity. Global Ecology and Biogeography, 22, 878-888.
[33] Naeem S, Wright JP ( 2003). Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecology Letters, 6, 567-579.
[34] Niu KC, Liu YN, Shen ZH, He FL, Fang JY ( 2009). Community assemble: The relative important of neutral theory and niche theory. Biodiversity Science, 17, 579-593.
[ 牛克昌, 刘怿宁, 沈泽昊, 何芳良, 方精云 ( 2009). 群落构建的中性理论和生态位理论. 生物多样性, 17, 579-593.]
[35] Paine CET, Baraloto C, Chave J, Hérault B ( 2011). Functional traits of individual trees reveal ecological constraints on community assembly in tropical rain forests. Oikos, 120, 720-727.
[36] Pärtel M, Szava-Kovats R, Zobel M ( 2011). Dark diversity: Shedding light on absent species. Trends in Ecology & Evolution, 26, 124-128.
[37] Pearse WD, Jones A, Purvis A ( 2013). Barro Colorado Island’s phylogenetic assemblage structure across fine spatial scales and among clades of different ages. Ecology, 94, 2861-2872.
[38] Ricklefs RE ( 1987). Community diversity: Relative roles of local and regional processes. Science, 235, 206-207.
[39] Spasojevic MJ, Suding KN ( 2012). Inferring community assembly mechanisms from functional diversity patterns: The importance of multiple assembly processes. Journal of Ecology, 100, 652-661.
[40] Srivastava DS ( 1999). Using local-regional richness plots to test for species saturation: Pitfalls and potentials. Journal of Animal Ecology, 68, 1-16
[41] Swenson NG ( 2011). Phylogenetic beta diversity metrics, trait evolution and inferring the functional beta diversity of communities. PLOS ONE, 6, e21264. DOI: 10.137/journal.pone.0021264.
[42] Swenson NG ( 2013). The assembly of tropical tree communities-‌the advances and shortcomings of phylogenetic and functional trait analyses. Ecography, 36, 264-276.
[43] Swenson NG, Enquist BJ ( 2009). Opposing assembly mechanisms in a Neotropical dry forest: Implications for phylogenetic and functional community ecology. Ecology, 90, 2161-2170.
[44] Swenson NG, Enquist BJ, Pither J, Thompson J, Zimmerman JK ( 2006). The problem and promise of scale dependency in community phylogenetics. Ecology, 87, 2418-2424.
[45] Swenson NG, Erickson DL, Mi X, Bourg NA, Forero-Montaña J, Ge XJ, Howe R, Lake JK, Liu XJ, Ma KP, Pei NC, Thomson J, Uriarte M, Wolf A, Wright SJ, Ye WH, Zhang JL, Zimmerman JK, Kress WJ ( 2012). Phylogenetic and functional alpha and beta diversity in temperate and tropical tree communities. Ecology, 93, S112-S125.
[46] Vamosi SM, Heard SB, Vamosi JC, Webb CO ( 2009). Emerging patterns in the comparative analysis of phylogenetic community structure. Molecular Ecology, 18, 572-592.
[47] Wang XX, Long WX, Yang XB, Xiong MH, Kang Y, Huang J, Wang X, Hong XJ, Zhou ZL, Lu YQ, Fang J, Li SX ( 2016). Patterns of plant diversity within and among three tropical cloud forest communities in Hainan Island. Chinese Journal of Plant Ecology, 40, 469-479.
[ 王茜茜, 龙文兴, 杨小波, 熊梦辉, 康勇, 黄瑾, 王旭, 洪小江, 周照骊, 陆雍泉, 方精, 李时兴 ( 2016). 海南岛3个林区热带云雾林植物多样性变化. 植物生态学报, 40, 469-479.]
[48] Webb CO, Ackerly DD, Kembel SW ( 2008). Phylocom: Software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics, 24, 2098-2100.
[49] Webb CO, Ackerly DD, Mcpeek MA, Donoghue MJ ( 2002). Phylogenies and community ecology. Annual Review of Ecology and Systematics, 33, 475-505.
[50] Weiher E, Keddy CPA ( 1998). Community assembly rules, morphological dispersion, and the coexistence of plant species. Oikos, 81, 309-322.
[51] Yang J, Zhang G, Ci X, Swenson NG, Cao M, Sha LQ, Li J, Baskin CC, Slik JWF, Lin LX ( 2014). Functional and phylogenetic assembly in a Chinese tropical tree community across size classes, spatial scales and habitats. Functional Ecology, 28, 520-529.
[52] Zobel M, Scheiner S ( 2016). The species pool concept as a framework for studying patterns of plant diversity: Official organ of the International Association for Vegetation Science. Journal of Vegetation Science, 27, 8-18.
[1] XU Jin-Shi,CHAI Yong-Fu,LIU Xiao,YUE Ming,GUO Yao-Xin,KANG Mu-Yi,LIU Quan-Ru,ZHENG Cheng-Yang,JI Cheng-Jun,YAN Ming,ZHANG Feng,GAO Xian-Ming,WANG Ren-Qing,SHI Fu-Chen,ZHANG Qin-Di,WANG Mao. Community assembly, diversity patterns and distributions of broad-leaved forests in North China [J]. Chin J Plant Ecol, 2019, 43(9): 732-741.
[2] TANG Li-Li,ZHANG Mei,ZHAO Xiang-Lin,KANG Mu-Yi,LIU Hong-Yan,GAO Xian-Ming,YANG Tong,ZHENG Pu-Fan,SHI Fu-Chen. Species distribution and community assembly rules of Juglans mandshurica in North China [J]. Chin J Plant Ecol, 2019, 43(9): 753-761.
[3] SHI Jing-Jing,ZHAO Ming-Fei,WANG Yu-Hang,XUE Feng,KANG Mu-Yi,JIANG Yuan. Community assembly of herbaceous layer of the planted forests in the central Loess Plateau, China [J]. Chin J Plant Ecol, 2019, 43(9): 834-842.
[4] CHAI Yong-Fu,XU Jin-Shi,LIU Hong-Yan,LIU Quan-Ru,ZHENG Cheng-Yang,KANG Mu-Yi,LIANG Cun-Zhu,WANG Ren-Qing,GAO Xian-Ming,ZHANG Feng,SHI Fu-Chen,LIU Xiao,YUE Ming. Species composition and phylogenetic structure of major shrublands in North China [J]. Chin J Plant Ecol, 2019, 43(9): 793-805.
[5] QIN Hao,ZHANG Yin-Bo,DONG Gang,ZHANG Feng. Altitudinal patterns of taxonomic, phylogenetic and functional diversity of forest communities in Mount Guandi, Shanxi, China [J]. Chin J Plant Ecol, 2019, 43(9): 762-773.
[6] Gui Xujun, Lian Juyu, Zhang Ruyun, Li Yanpeng, Shen Hao, Ni Yunlong, Ye Wanhui. Vertical structure and its biodiversity in a subtropical evergreen broad- leaved forest at Dinghushan in Guangdong Province, China [J]. Biodiv Sci, 2019, 27(6): 619-629.
[7] HAO Shu-Jun, LI Xiao-Yu, HOU Man-Man, ZHAO Xiu-Hai. Spatial variations of community functional traits at different successional stages in temperate forests of Changbai Mountains, Northeast China [J]. Chin J Plant Ecol, 2019, 43(3): 208-216.
[8] WEN Chun,JIN Guang-Ze. Effects of functional diversity on productivity in a typical mixed broadleaved-Korean pine forest [J]. Chin J Plant Ecol, 2019, 43(2): 94-106.
[9] LIU Jin-Liang, YU Ming-Jian. Community assembly processes in fragmented forests and its testing methods [J]. Chin J Plant Ecol, 2019, 43(11): 929-945.
[10] Weng Changlu,Zhang Tiantian,Wu Donghao,Chen Shengwen,Jin Yi,Ren Haibao,Yu Mingjian,Luo Yuanyuan. Drivers and patterns of α- and β-diversity in ten main forest community types in Gutianshan, eastern China [J]. Biodiv Sci, 2019, 27(1): 33-41.
[11] Dexin Sun, Xiang Liu, Shurong Zhou. Dynamical changes of diversity and community assembly during recovery from a plant functional group removal experiment in the alpine meadow [J]. Biodiv Sci, 2018, 26(7): 655-666.
[12] Xiaorong Huang. Relationship between plant functional diversity and productivity of Pinus massoniana plantations in Guangxi [J]. Biodiv Sci, 2018, 26(7): 690-700.
[13] Hou Qinxi, Ci Xiuqin, Liu Zhifang, Xu Wumei, Li Jie. Assessment of the evolutionary history of Lauraceae in Xishuangbanna National Nature Reserve using DNA barcoding [J]. Biodiv Sci, 2018, 26(3): 217-228.
[14] SHI Guo-Xi, WANG Wen-Ying, JIANG Sheng-Jing, CHENG Gang, YAO Bu-Qing, FENG Hu-Yuan, ZHOU Hua-Kun. Effects of the spreading of Ligularia virgaurea on soil physicochemical property and microbial functional diversity [J]. Chin J Plan Ecolo, 2018, 42(1): 126-132.
[15] Yunfeng Song, Shengwen Chen, Wei Wang, Jianping Yu, Haiyuan Qian, Yunquan Wang, Lei Chen, Xiangcheng Mi, Haibao Ren, Duo Ye, Jianhua Chen, Keping Ma. Effects of negative density dependence and habitat filtering on the functional diversity of seedlings in the subtropical forest of Gutianshan [J]. Biodiv Sci, 2017, 25(9): 959-965.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Liu Ying-di. The Role of Ultrastructure in Algal Systematics[J]. Chin Bull Bot, 1990, 7(04): 18 -23 .
[2] Fan Guo-qiang and Jiang Jian-ping. Study on the Methods of Extraction of Protein from Paulownia Leaves[J]. Chin Bull Bot, 1997, 14(03): 61 -64 .
[3] Tong Zhe and Lian Han-ping. Cryptochrome[J]. Chin Bull Bot, 1985, 3(02): 6 -9 .
[4] Huang Ju-fu and Luo Ai-ling. The Advances of the Studies on Extraction of FeMoco from Nitrogenase Molybdenum-Iron Protein[J]. Chin Bull Bot, 1991, 8(03): 19 -25 .
[5] Hsu Rong-jiang Gu Wen-mao Gao Jing-cheng and Peng Chang-ming. Inhibitory Effect of High CO2 and Low O2 Tension on Ethylene Evolution in Apples[J]. Chin Bull Bot, 1984, 2(01): 29 -31 .
[6] Zou Shu-hua;Zhao Shu-wen and Xu Bao. Electropheresis Profiles of Esterase Isozymes in Different Types of Soybean[J]. Chin Bull Bot, 1985, 3(06): 18 -20 .
[7] . [J]. Chin Bull Bot, 1999, 16(增刊): 49 -52 .
[8] Chi Tingfei;Shi Xiaofang;Huang Ruzhu;Zheng Xiangyun;Yuan Xiangning and Wu Dangjian. A Preliminary Study on the Chemical Constituents of the Leave Oil in prunus zippeliana Mig[J]. Chin Bull Bot, 1986, 4(12): 44 -45 .
[9] Houqing Zeng, Yaxian Zhang, Shang Wang, Xiajun Zhang, Huizhong Wang, Liqun Du. Calcium/calmodulin-mediated Signal Transduction System in Plants[J]. Chin Bull Bot, 2016, 51(5): 705 -723 .
[10] Zhu Zhi-qing. Abbreviations for some Commonly Used Terms in Ultrastructures of Plant Cells[J]. Chin Bull Bot, 1984, 2(04): 57 -58 .